Phototrophic Lactate Utilization by Rhodopseudomonas palustris Is Stimulated by Coutilization with Additional Substrates

Abstract

The phototrophic purple nonsulfur bacterium Rhodopseudomonas palustris is known for its metabolic versatility and is of interest for various industrial and environmental applications. Despite decades of research on R. palustris growth under diverse conditions, patterns of R. palustris growth and carbon utilization with mixtures of carbon substrates remain largely unknown. R. palustris readily utilizes most short-chain organic acids but cannot readily use lactate as a sole carbon source. Here we investigated the influence of mixed-substrate utilization on phototrophic lactate consumption by R. palustris. We found that lactate was simultaneously utilized with a variety of other organic acids and glycerol in time frames that were insufficient for R. palustris growth on lactate alone. Thus, lactate utilization by R. palustris was expedited by its coutilization with additional substrates. Separately, experiments using carbon pairs that did not contain lactate revealed acetate-mediated inhibition of glycerol utilization in R. palustris. This inhibition was specific to the acetate-glycerol pair, as R. palustris simultaneously utilized acetate or glycerol when either was paired with succinate or lactate. Overall, our results demonstrate that (i) R. palustris commonly employs simultaneous mixed-substrate utilization, (ii) mixed-substrate utilization expands the spectrum of readily utilized organic acids in this species, and (iii) R. palustris has the capacity to exert carbon catabolite control in a substrate-specific manner. IMPORTANCE Bacterial carbon source utilization is frequently assessed using cultures provided single carbon sources. However, the utilization of carbon mixtures by bacteria (i.e., mixed-substrate utilization) is of both fundamental and practical importance; it is central to bacterial physiology and ecology, and it influences the utility of bacteria as biotechnology. Here we investigated mixed-substrate utilization by the model organism Rhodopseudomonas palustris. Using mixtures of organic acids and glycerol, we show that R. palustris exhibits an expanded range of usable carbon substrates when provided substrates in mixtures. Specifically, coutilization enabled the prompt consumption of lactate, a substrate that is otherwise not readily used by R. palustris. Additionally, we found that R. palustris utilizes acetate and glycerol sequentially, revealing that this species has the capacity to use some substrates in a preferential order. These results provide insights into R. palustris physiology that will aid the use of R. palustris for industrial and commercial applications.

Development of a low-cost culture medium for the rapid production of plant growth-promoting Rhodopseudomonas palustris strain PS3

“…Molasses is a by-product of the sugar manufacturing process and may be obtained from beet or sugarcane; it contains abundant saccharides (such as sucrose, glucose, and fructose) and small amounts of organic acids (such as acetic acid and lactic acid) [50,51]. It has been reported that R. palustris biomass production is stimulated by the co-utilization of multiple carbon sources [52]. Similar phenomenon was also observed in other microorganisms.…”

“…It has been reported that R . palustris biomass production is stimulated by the co-utilization of multiple carbon sources [ 52 ]. Similar phenomenon was also observed in other microorganisms.…”

Enhanced CO2 capture for photosynthetic lycopene production in engineered Rhodopseudomonas palustris, a purple nonsulfur bacterium

“…23,57 The oxidation value glycerol is −0.67, which is more reduced than the biomass of R. palustris with an oxidation value of −0.5. 39,58 Therefore, R. palustris cannot grow anaerobically on glycerol alone unless it can dispose of the excess electrons associated with this compound, which was demonstrated by the non-growth of R. palustris with 10 mM or 20 mM glycerol supplied as the sole carbon source (Fig. 6C).…”

Characteristics and Application of Rhodopseudomonas palustris as a Microbial Cell Factory

“…Seven different organic acid salts were individually added into the culture medium of methane-producing R. palustris as carbon sources, and the highest yield of methane was obtained when fumarate was added ( Fixen et al, 2016 ). R. palustris cannot readily use lactate as a sole carbon source, and coutilization with other substrates stimulated its consumption ( Govindaraju et al, 2019 ). When different concentrations (2–10 mmol/L) of lactate were added into the culture medium, different hydrogen yields were obtained ( Lazaro et al, 2017 ).…”